Powdery Mildew (PM) in watermelons (Citrullus lanatus L.) is a fungal disease caused by Podosphaera xanthii (castagne) U. Braun & N. Shishkoff. In the present study, race of watermelon PM present in South Korea was confirmed, and genetic inheritance of resistance to this PM race was determined from the cultivar ‘Arka Manik’. In addition, a molecular marker tightly linked to this resistance locus was developed by bulked segregant analysis (BSA). The result of bioassay tested on a set of melon differential genotypes indicated that the pathotype of P. xathii predominating in watermelon production fields in South Korea was either race 1W or another race different from race 2W. Inheritance of PM resistance was studied from F2, F2:3, and reciprocal backcross generations derived from ‘Arka Manik’ (resistant cultivar) x HS3355 (susceptible line). The segregation ratios observed in these generations indicated that resistance to PM in ‘Arka Manik’ is conditioned by a single incompletely dominant gene (Pm1.1). BSA of F2 plants using random amplification of polymorphic DNA (RAPD) was conducted to develop a DNA marker for selecting PM resistance. Among 5,393 loci scored, one polymorphic polymerase chain reaction (PCR) band (OPC11-483) was identified from RAPD primer OPC11. F2 generations were tested to confirm the frequency of cosegregation between resistance and OPC11-483. Cosegregation frequencies higher than 97% were observed. The marker OPC11-483 was converted to cleave amplification polymorphisms (CAPS-T/G) and a single nucleotide polymorphism (SNP) marker (MCA-A/G) using melting curve analysis on a real-time PCR platform. MCA-A/G marker genotyping of a wide range of susceptible breeding lines revealed that the marker allele of ‘Arka Manik’ was very unique in breeding population. This codominant SNP marker tightly linked to PM resistance can be efficiently utilized for marker-assisted selection in a breeding program that uses ‘Arka Manik’ as a resistance source.